Journal of Avian Biology 44: 001–010, 2013 doi: 10.1111/j.1600-048X.2013.00072.x © 2013 The Authors. Journal of Avian Biology © 2013 Nordic Society Oikos Subject Editor: Thoams Alerstam. Accepted 4 February 2013
Satellite telemetry reveals long-distance migration in the Asian great bustard Otis tarda dybowskii
A. E. Kessler, N. Batbayar, T. Natsagdorj, D. Batsuur’ and A. T. Smith
A. E. Kessler ([email protected]) and A. T. Smith, School of Life Sciences, Arizona State Univ., Tempe, AZ 85287, USA. – N. Batbayar, Dept of Microbiology and Plant Biology, Center for Spatial Analysis, Univ. of Oklahoma, Norman, ok 73019, USA. – D. Batsuur’ and T. Natsagdorj, Inst. of Biology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia.
The range of the great bustard stretches 10 000 km across Eurasia, one of the largest ranges of any threatened species. While movement patterns of the western subspecies of great bustard are relatively well-understood, this is the first research to monitor the movements of the more endangered Asian subspecies of great bustard through telemetry and to link a breeding population of Asian great bustards to their wintering grounds. Using Argos/GPS platform transmitter terminals, we identified the annual movement patterns of three female great bustards captured at their breeding sites in northern Mongolia. The 4000 km round-trip migration we have recorded terminated at wintering grounds in Shaanxi, China. This route is twice as long as has previously been reported for great bustards, which are among the heaviest flying birds. The journey was accomplished in approximately two months each way, at ground velocities of 48–98 km h21, and incorporated multiple and variable stopover sites. On their wintering grounds these birds moved itinerantly across relatively large home ranges. Our findings confirm that migratory behavior in this species varies longitudinally. This variation may be attributable to longitudinal gradients in seasonality and severity of winter across Eurasia. The distance and duration of the migratory route taken by great bustards breeding in Mongolia, the crossing of an international border, the incorporation of many stopovers, and the use of a large wintering territory present challenges to the conservation of the Asian subspecies of great bustard in this rapidly changing part of the world.
The range of the great bustard Otis tarda, a large lekking Able 1988). In general, migratory distance of great bustards bird, stretches from Manchuria to the Iberian Peninsula increases longitudinally across Europe from west to east, in across the grasslands and steppes of Eurasia (Isakov 1974, correspondence with severity of winter weather conditions Collar 1996). The two subspecies of great bustard, European and the degree of seasonality. A variety of short seasonal (O. t. tarda) and Asian (O. t. dybowskii) are geographically movements have been described in Spanish populations. isolated and differ in coloration of neck, wing coverts and These include post-breeding migrations by some males of rectrices, patterning on the back, and extent of specialized up to 196 km, the distance of which may be dependent on display plumes on the chin and neck (Ivanov et al. 1951, climatic and habitat variables (Alonso et al. 2001, 2009). Johnsgard 1991). While populations of the nominal subspe- Some females make autumn/winter movements of up to 110 cies are listed as Vulnerable (VU) worldwide by IUCN km (Alonso et al. 2000, Palacín et al. 2009); these migrations (BirdLife International 2012), only 1200–2200 Asian great are culturally transmitted and condition-dependent (Palacín bustards remain and this subspecies is Red-listed across its et al. 2011). range of Russian South Siberia, Mongolia and China Great bustards in central Europe tend to be sedentary, (Tseveenmyadag 2003, Goroshko 2008). Breeding grounds though short migrations by some populations, or some in Mongolia now represent the stronghold for this subspecies individuals in a population, have been observed (Bankovics (Alonso and Palacín 2010). Clarification of threats to the and Széll 2006). Irregular irruptive movements of up to subspecies and its natural history parameters, particularly in 650 km have been recorded for these populations in response Mongolia, is identified as a priority for its conservation to severe winter weather (Faragó 1990, Block 1996, Streich (Boldbaatar 1997, Chan and Goroshko 1998). et al. 2006). Detailed movement studies have not previously been Populations of European great bustards on the Lower undertaken on Asian great bustards, but data from radio and Volga River in Russia – the most easterly populations for satellite tracking of the European subspecies indicate that which tracking data are available – are mostly migratory. great bustards display a wide range of migratory behaviors, Females monitored via satellite telemetry traveled 1100 including both partial and differential migration (Terrill and km over the course of approximately one week to winter in
EV-1 southeast Ukraine (Oparina et al. 2001, Watzke et al. 2001, of capture within 15–30 min. The PTT and harness repre- Khrustov 2009). sent approximately 2% of the females’ body weight, which Our group investigated the migratory behavior of Asian falls within the range of loads recommended by Kenward great bustards in north central Mongolia, approximately (2001). 4000 km east and 200 km south of the Volga populations. Each PTT transmitted GPS data ( 18 m accuracy) Given the severely continental climate of northern Mongo- by radio signal to the Argos system (maintained by CLS, lia, we predicted that distance migrated would be farther Toulouse, France) deployed on satellites. Duty cycles were than observed in European populations, in correspondence tailored to maximize the number of GPS locations transmit- with the longitudinal trends noted above. Here we present ted, with the length of day and strength of solar charge to the first data on complete annual movements of this subspe- the battery as limiting factors. Locations were recorded every cies: the long-distance round-trip migrations of three female two hours from 6:00 to 20:00 in spring and fall, from 4:00 Asian great bustards. to 22:00 in summer, and from 7:00 to 19:00 in winter. PTTs also reported speed of movement ( 1 km h1 accuracy at speeds 40 km h1). Upon receipt of a series of radio trans- Methods missions, the Argos system also estimates the location of the PTT using Doppler shift calculations, which are transferred Research was carried out on breeding populations of great in a separate data frame. bustards in east Khövsgöl Aimag, Mongolia (approximately A comparison of the movements of individual tagged 50°N, 101°E). Birds were found in valleys dominated by birds to each other, and to records of bustard migration at low-intensity agriculture (primarily summer wheat) and geographically similar locations, did not yield observations livestock herding by nomadic pastoralists. In this region of consistent delays by any individual. We also did not of forest-steppe, winters are severe, with average January observe correspondence between failure to breed and timing temperatures around 30°C (Inst. Geografii – Sibirskoe of spring arrival, which would indicate strong transmitter Otdelenie 1989). Nights and cold fronts in winter bring low effects (Barron et al. 2010). temperatures of 40 to 50°C. Routes were plotted and distances between points All work was carried out under permits issued by the calculated using ArcGIS 10. Minimum convex poly- Mongolian Ministry of Nature, Environment, and Tourism gons and kernel density estimations were created using (no. 4/730, 4/1813, 6/1650) and using methods approved Geospatial modelling environment (Beyer 2011). Departure by the Arizona State Univ. Institutional Animal Care and and arrival dates were determined primarily through scru- Use Committee (no. 07-924R). We captured one female in tiny of GPS-quality transmissions. We used Doppler-shift 2007 and two additional females in 2008 by spotlighting calculated locations when those allowed us to narrow the (Giesen et al. 1982, Seddon et al. 1999, Geyser 2000). range of dates of a bird’s arrival or departure in the absence Each bird was fitted with a solar-powered 70 g Argos/ of GPS-quality data. GPS platform transmitter terminal (‘PTT’) using a custom- fit backpack harness (modified from Osborne and Osborne 1998, Alonso et al. 2001). Stretchable silicone rope was Results threaded through bunched teflon ribbon to create a durable harness capable of adjusting to weight changes. The straps All three female birds were roughly the same weight at of the backpack cross at the breast, where they were stitched capture (Table 1). Birds no. 01 and no. 03 were captured to ensure that the harness did not shift location. Points at in the same valley; bird no. 02 was captured in a valley which the harness was threaded through the transmitter were 50 km distant. Data presented are of migratory movements stabilized with instant glue. Birds were released at the site from date of capture (Table 1) through 1 June 2009.
Table 1. Migratory activity recorded for three female great bustards Otis tarda dybowskii captured in north central Mongolia and harnessed with Argos/GPS satellite transmitters.
Mean ground Capture Distance Start End Duration Mean km Number of speed SD Bird ID date/weight Season flown (km) date date (days) flown d1 GPS points (km h1) n* 01 14 Jun 2007 fall 2007 1954 13–16 Oct 4–12 Dec 49–60 33–40 56 59 2 3 3400 g 01 - fall 2008 1852 17–19 Oct 4–6 Nov 16–20 93–116 19 59 6 5 02 27 Jun 2008 fall 2008 1836 12 Oct 31 Oct 19 97 56 87 10 3 3500 g 03 10 Jun 2008 fall 2008 2044 17 Oct 18–20 Dec 62–64 32–33 205 76 12 5 3600 g 01 spring 2008 1966 24–26 Mar 28–31 May 63–68 29–31 39 62 1 01 spring 2009 1932 12–14 Mar 1 Jun 79–81 24 80 NA – 02 spring 2009 1860 5 Apr 9–13 May 34–38 49–55 52 80 6 2 03 spring 2009 2100 5 Apr 9 Jun 65 32 323 60 9 8 *number of in-flight observations used to calculate mean flight velocity.
EV-2 Due to radio interference typical in eastern Siberia and The spring and fall migratory routes of bird 03 exhibited China and poor battery charge especially during winter the most variation of the three birds tracked, with a maxi- months, not all logged GPS data were ultimately received mum divergence of approximately 170 km (Fig. 2). This bird by the Argos system. The greatest distance between any two also took a detour of 60 km in northern Mongolia before successively received GPS points was approximately 1000 returning to her primary lek in spring 2009. km, from Khövsgöl Aimag in Mongolia to the southern border of Mongolia, over a period of six days (bird no. 01, Duration fall 2008). Each female migrated from Khövsgöl Province in north- Though distances traveled were similar among birds and sea- ern Mongolia in a southeastern direction (approximately sons, we found five-fold variation among the three birds in 140°) to wintering spots near Xi’an city in Shaanxi Prov- the duration of migration. Average duration of a one-way ince, China (Fig. 1–3). Data indicate that the marked birds trip was approximately two months (Table 1). In three of traveled independently of one another. Fall routes deviated four cases, spring migration lasted longer than that bird’s from spring routes, but a consistent loop directionality was previous autumn migration. In the case of bird 01, spring not detected. Average distance migrated was approximately 2009 migration was almost two months longer than the 2000 km one-way, and was similar among birds and seasons preceding fall migration (Table 1). (Table 1). When in flight bird 02 regularly achieved speeds 30% The migratory route of bird 01 in 2008 was similar to her greater than the other two birds, with a maximum ground route in 2007 (Fig. 1). In spring 2009 bustard 01 also per- speed of 98 km h1. The duration of her migrations was formed a 50 km roundtrip detour in the direction of another approximately half that of the other two birds (Table 1). known lek, where she spent 4–8 d before returning along the Minimum ground speed recorded was 48 km h1 for bird 03 same path to resume her route northward. in spring 2009.
Figure 1. Map (UTM 47N projection) of the autumn 2007 (o), spring 2008 (), autumn 2008 (▴) and spring 2009 (x) migratory routes of female great bustard Otis tarda dybowskii no. 01. Each vertex represents a GPS-quality stop location reported by the transmitter. GPS locations during flight were used to construct the path, but are not shown as vertices.
EV-3 Figure 2. Map (UTM 47N projection) of the autumn 2008 (o) and spring 2009 () migratory routes of female great bustard Otis tarda dybowskii no. 03. Each vertex represents a GPS-quality stop location reported by the transmitter. GPS locations during flight were used to construct the path, but are not shown as vertices.
Stopover sites range was recorded for bird 01 in winter 2008; this dataset also included the fewest observations and a gap in data recep- The bustards we monitored used multiple and varied stop- tion of 107 d (Table 2). Bird 03 gradually moved eastward over sites, and it is likely that additional locations in which during the winter months, such that her first major north- the birds stopped were not detected because of failed trans- ward movement was 90 km east of her last major southward missions. We did not find fidelity to specific stopover locali- movement (Table 2). Bird 02 also spent much of the winter ties. Most routes included a stop on the outskirts of Bayanur, moving gradually 50 km to the northeast. an agricultural oasis in Nei Mongol, China, but stopovers Though birds 01 and 03 summer at the same lekin there were spread across 130 km. Individuals occupied some northern Mongolia, their wintering ranges did not overlap stopovers for only 1–2 d and rarely took longer stops. Stops (Fig. 4). The ranges of birds 02 and 03 overlapped (Fig. 4), of approximately 10 d were recorded in Khishig-Öndör sum but the core areas used by each bird differed (Fig. 5). In of Bulgan Aimag and Tarialan sum of Khövsgöl Aimag, 2008, bird 01 wintered 40 km north of the range she used in Mongolia, and Ordos Prefecture and the Bayanur oasis in the previous winter. Nei Mongol, China. One stop of 45 d was recorded for bird 03 in the Bayanur oasis. Discussion Wintering sites Migratory ecology These bustards overwintered in agricultural fields near the confluence of the Wei and Yellow Rivers in Shaanxi Province Geographic variation in migratory route of China. Individuals tended to progress eastward through a The migration routes we observed for Asian great bustards series of non-repeated sites over the course of winter months, were twice as long as have previously been described for this resulting in a large overall winter range (Fig. 4). The smallest species in the Lower Volga (Oparina et al. 2001) and 18 times
EV-4 Figure 3. Map (UTM 47N projection) of the autumn 2008 (o) and spring 2009 () migratory routes of female great bustard Otis tarda dybowskii no. 02. Each vertex represents a GPS-quality stop location reported by the transmitter. GPS locations during flight were used to construct the path, but are not shown as vertices.
longer than those documented for female great bustards in Severity of winter weather increases longitudinally Spain (Alonso et al. 2000, Palacín et al. 2009). Migratory not only across Europe, but also into landlocked areas distances thus increase longitudinally from west to east of central Eurasia (Borisov 1959). Mean low January across the range of this species. Similar geographic variation temperatures are 30°C cooler and lowest recorded January has been reported in the migration of other Palearctic bus- temperatures are 36°C cooler in Khövsgöl than Madrid tard species, which exhibit greater proclivity to migrate and (Linés Escardó 1970, Lydolph 1977, World Meteorologi- undertake migrations of greater distance in the eastern por- cal Organization 1996). Seasonality increases longitudinally tion of their ranges (Roselaar 1980, Combreau et al. 2011). across this distance, with 18°C greater difference between Murphy (1985) hypothesized that species exhibit mean July and mean January temperatures in Khövsgöl than biogeographical patterns reflecting increasing seasonality in Madrid (World Meteorological Organization 1996). Thus, longitudinally from west to east across the western Palearc- the longitudinal trend toward increased migratory behavior tic. Meiri et al. (2005) found western Palearctic bird species in great bustards is consistent with Murphy’s hypothesis (127 species in 14 orders) to show a greater tendency to and the biogeographical findings of Meiri et al. (2005) migrate in eastern portions than in western portions of their and Siriwardena and Wernbaum (2002), and Asian great ranges. Geographic variation has also been noted within bustards represent the extreme of a longitudinal continuum bird species in the UK, where birds from areas with harsher of adaptation to severe climate. To put the degree of differ- climates made migrations of greater length than those from ence in climates into context, note that the mean annual regions with milder climates (Siriwardena and Wernham range in temperature anywhere in Spain is similar to the 2002). Further, migration distance has decreased in European mean daily range of temperature in our study region in bird species as winter severity lessens with climate change northern Mongolia during the breeding season (20°C; Linés (Visser et al. 2009). Escardó 1970, Lydolph 1977).
EV-5 Figure 4. Map (UTM 47N projection) of the minimum convex polygons encompassing GPS locations at which each great bustard was recorded over the winter. Watercourses and urbanized areas are shaded.
Given these observations and the tendency of otherwise Stopover and wintering grounds and fidelity sedentary central European great bustards to migrate in We did not observe stopover site fidelity in the great bus- adverse weather conditions (Streich et al. 2006), it is likely tards we monitored. This finding is in line with predictions that harsh continental winters drive the observed long-distance for optimal migration in species that are not habitat special- migration of Asian great bustards breeding on the Mongolian ists (Cantos and Tellería 1994), in that birds may reduce Plateau. Indeed, northerly and northwesterly winds arising energy expenditure by correcting for wind drift only when from the Siberian high-pressure system responsible for low approaching their final destination (Alerstam 1979, Catry winter temperatures in the region (Lydolph 1977, Gong and et al. 2004). Ho 2002) may facilitate the southeasterly migration of great Our study is the first to link a breeding population of bustards. Variation in weather and forage conditions may Asian great bustards to their wintering grounds. Though we cause variation in timing of migration of bustards from year to studied bustards breeding in north central Mongolia, addi- year (Kozlova 1975, Tseveenmyadag 2003). tional breeding populations are scattered across central and In contrast to the severe winter temperatures described above eastern Mongolia (Tseveenmyadag 2003) and northeastern for Khövsgöl Aimag, mean January temperatures in Xi’an, China (Gao et al. 2008). Given that these eastern breeding China, remain around 0°C (Watts 1969, World Meteorological populations are subject to similar climatic and wind patterns, Organization 1996). Through migration, great bustards may we hypothesize that the migratory routes of great bustards in avoid not only cold temperatures, but also conditions of food eastern Mongolia parallel the southeasterly routes we have shortage due to snow cover (Streich et al. 2006). identified for central Mongolian bustards. If this hypothesis
Table 2. Wintering areas in China for three great bustards captured in northern Mongolia. MCP stands for minimum convex polygon.
Number of Significant gaps Area of Area of 80% kernel Maximum distance Bird ID Winter GPS points in data (days) MCP (km2) (km2) between points (km) Ground speed n* 01 2007–2008 49 12, 20, 18 401.7 63.7 51.7 61 1 01 2008–2009 26 107 86.1 35.8 29.6 NA – 02 2008–2009 217 11, 16, 10 1450.7 355.7 93.8 64 1 03 2008–2009 200 17, 14, 12 1967.6 723.2 95.4 54 1 *no. of in-flight measurements received.
EV-6 Figure 5. Map (UTM 47N projection) of 80% kernel density estimates of wintering areas used by each tagged great bustard. Watercourses and urbanized areas are shaded. proves true, the overall effect of Asian great bustard migra- The range of migratory rates we observed for Asian great tion would be a wide front gradually advancing through bustards overlapped with rates observed and expected for central and eastern Mongolia and China. other large-bodied birds, such as swans, Cygnus spp., and In contrast to behavior described in Spanish popula- geese, Anser spp. (Pennycuick 1989, Hedenström and Aler- tions of great bustards, we observed winter site fidelity only stam 1998). The houbara bustard Chlamydotis undulata, a at a regional scale. While winter home ranges of female sister species (Broders et al. 2003) which also breeds in cen- bustards in Spain were less than 5 km in diameter (Alonso tral and inner Asia, exhibits migratory behavior similar to et al. 2000), the bustards we monitored occupied a series of that we have observed in Asian great bustards (Combreau locations across 30 to 95 km. et al. 1999, Judas et al. 2006). The shorter duration of fall migration, as compared to Migratory flight speed and duration spring migration, undertaken by our tagged bustards con- The bustards we monitored spent approximately one-third trasts with the general trend observed in European and of the year on their migratory path. Active flight repre- African migrants (Newton 2008, Yohannes et al. 2009). sented only 2–6% of the duration of each bird’s migratory However, a shorter fall migration may be typical in less period. This extended migration period may be attributable well-studied inner Asia, where migrants face steeper envi- to physiological and ecological constraints in heavier birds. ronmental gradients in spring (Raess 2008). Further, Asian Larger individuals are expected to stop more frequently and great bustards may be migrating with the aid of tail winds in spend relatively more time at stopovers (Pennycuick 1989, fall, whereas in Europe the converse is the case (Kemp et al. Klaassen 1996, Hedenström and Alerstam 1998). A slow 2010). It has also been suggested that long spring stopovers migration speed is typical of species which migrate later in among another bustard species (houbara) may allow females autumn, and bustards are among the last migrants to depart to store reserves to be used for egg production immediately northern Mongolia (Alerstam and Lindström 1990, Ellegren upon arrival at the breeding grounds (Tourenq et al. 2004). 1993, Yohannes et al. 2009). Finally, species which migrate diurnally, as do bustards, typically migrate more slowly than Conservation across the migratory range nocturnal migrants, most likely because they are limited to daylight hours for both flying and foraging (Hildén and The female Asian great bustards we monitored spent two- Saurola 1982). thirds of the year at migratory stopover sites and wintering
EV-7 grounds. Given the large territory over which Asian great References bustards range annually, the variety of threats they face, their use of human-dominated landscapes and nomadic behav- Alerstam, T. 1979. Wind as selective agent in bird migration. ior outside of the breeding season, it is clear that the con- – Ornis Scand. 10: 76–93. servation of Asian great bustards will require a broad-scale Alerstam, T. and Lindström, Å. 1990. Optimal bird migration: the strategy and the integrated management of habitat between relative importance of time, energy and safety. – In: Gwinner, E. (ed.), Bird migration: physiology and ecophysiology. governmental agencies across provincial and international Springer, pp. 331–351. boundaries as well as the cooperation of local stakeholders Alonso, J. C. and Palacín, C. A. 2010. The world status and pop- (Boyd et al. 2008, Yorio 2009). ulation trends of the great bustard (Otis tarda): 2010 update. 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